Green fluorescent protein - Tagged HCV non-enveloped capsid like particles: Development of a new tool for tracking HCV core uptake

Biochimie

Volumn 91, Issue 7, 2009, Pages 903-915

  Katsarou, Konstantina ^a   Serti, Elisavet ^a   Tsitoura, Panagiota ^a   Lavdas, Alexandros A ^a   Varaklioti, Agoritsa ^b   Pickl Herk, Angela Maria ^c   Blaas, Dieter ^c   Oz Arslan, Devrim ^a   Zhu, Rong ^d   Hinterdorfer, Peter ^d   Mavromara, Penelope ^a   Georgopoulou, Urania ^a  

^a HELLENIC PASTEUR INSTITUTE   (Greece)

^b LAIKO GENERAL HOSPITAL   (Greece)

^c MEDICAL UNIVERSITY OF VIENNA   (Austria)

^d JOHANNES KEPLER UNIVERSITY LINZ   (Austria)

Author keywords

Cellular uptake; Fluorescent non enveloped capsid like particle; Hepatitis C virus

Indexed keywords

CORE PROTEIN; ENHANCED GREEN FLUORESCENT PROTEIN; NANOSPHERE; VIRUS ENVELOPE PROTEIN; VIRUS GLYCOPROTEIN;

ANIMAL CELL; ARTICLE; ATOMIC FORCE MICROSCOPY; B LYMPHOCYTE; CELL DIFFERENTIATION; CELL FATE; CELL TRANSPORT; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTRON MICROSCOPY; FLUORESCENCE ACTIVATED CELL SORTING; GENE DELETION; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; INSECT CELL; LEUKEMIA CELL; LIVER CELL; MACROPHAGE; MONOCYTE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TARGET CELL; VIRUS CAPSID; VIRUS CORE; VIRUS GENOME; VIRUS PARTICLE; VIRUS TRANSMISSION;

B-LYMPHOCYTES; CAPSID; CELL LINE, TUMOR; GREEN FLUORESCENT PROTEINS; HEPACIVIRUS; HEPATOCYTES; HUMANS; MONOCYTES; RECOMBINANT FUSION PROTEINS; T-LYMPHOCYTES; VIRAL CORE PROTEINS; VIRUS INTERNALIZATION;

HEPATITIS C VIRUS; HEXAPODA; MIRIDAE;

EID: 65749088478     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2009.04.016     Document Type: Article

References (44)

1. Houghton M. Hepatitis C Viruses. In: Knipe D.M., Fields B.N., and Howley P.M. (Eds). Fields Virology. third ed. vol. 1 (1996), Lippincott-Raven Publishers, Philadelphia 1035-1058
2. Andre P., Perlemuter G., Budkowska A., Brechot C., and Lotteau V. Hepatitis C virus particles and lipoprotein metabolism. Semin. Liver Dis. 25 (2005) 93-104
3. Maillard P., Krawczynski K., Nitkiewicz J., Bronnert C., Sidorkiewicz M., Gounon P., Dubuisson J., Faure G., Crainic R., and Budkowska A. Nonenveloped nucleocapsids of hepatitis C virus in the serum of infected patients. J. Virol. 75 (2001) 8240-8250
4. Iwai A., Marusawa H., Takada Y., Egawa H., Ikeda K., Nabeshima M., Uemoto S., and Chiba T. Identification of novel defective HCV clones in liver transplant recipients with recurrent HCV infection. J. Viral Hepat. 13 (2006) 523-531
5. Noppornpanth S., Smits S.L., Lien T.X., Poovorawan Y., Osterhaus A.D., and Haagmans B.L. Characterization of hepatitis C virus deletion mutants circulating in chronically infected patients. J. Virol. 81 (2007) 12496-12503
6. Yagi S., Mori K., Tanaka E., Matsumoto A., Sunaga F., Kiyosawa K., and Yamaguchi K. Identification of novel HCV subgenome replicating persistently in chronic active hepatitis C patients. J. Med. Virol. 77 (2005) 399-413
7. Tsitoura P., Georgopoulou U., Petres S., Varaklioti A., Karafoulidou A., Vagena D., Politis C., and Mavromara P. Evidence for cellular uptake of recombinant hepatitis C virus non-enveloped capsid-like particles. FEBS Lett. 581 (2007) 4049-4057
8. Charpilienne A., Nejmeddine M., Berois M., Parez N., Neumann E., Hewat E., Trugnan G., and Cohen J. Individual rotavirus-like particles containing 120 molecules of fluorescent protein are visible in living cells. J. Biol. Chem. 276 (2001) 29361-29367
9. Finke S., Brzozka K., and Conzelmann K.K. Tracking fluorescence-labeled rabies virus: enhanced green fluorescent protein-tagged phosphoprotein P supports virus gene expression and formation of infectious particles. J. Virol. 78 (2004) 12333-12343
10. Gilbert L., Toivola J., Lehtomaki E., Donaldson L., Kapyla P., Vuento M., and Oker-Blom C. Assembly of fluorescent chimeric virus-like particles of canine parvovirus in insect cells. Biochem. Biophys. Res. Commun 313 (2004) 878-887
11. Gilbert L., Toivola J., Valilehto O., Saloniemi T., Cunningham C., White D., Makela A.R., Korhonen E., Vuento M., and Oker-Blom C. Truncated forms of viral VP2 proteins fused to EGFP assemble into fluorescent parvovirus-like particles. J. Nanobiotechnology 4 (2006) 13
12. Lambert C., Thome N., Kluck C.J., and Prange R. Functional incorporation of green fluorescent protein into hepatitis B virus envelope particles. Virology 330 (2004) 158-167
13. Lux K., Goerlitz N., Schlemminger S., Perabo L., Goldnau D., Endell J., Leike K., Kofler D.M., Finke S., Hallek M., and Buning H. Green fluorescent protein-tagged adeno-associated virus particles allow the study of cytosolic and nuclear trafficking. J. Virol. 79 (2005) 11776-11787
14. Inchauspe G., Zebedee S., Lee D.H., Sugitani M., Nasoff M., and Prince A.M. Genomic structure of the human prototype strain H of hepatitis C virus: comparison with American and Japanese isolates. Proc. Natl. Acad. Sci. U.S.A. 88 (1991) 10292-10296
15. McLauchlan J., Lemberg M.K., Hope G., and Martoglio B. Intramembrane proteolysis promotes trafficking of hepatitis C virus core protein to lipid droplets. EMBO J. 21 (2002) 3980-3988
16. Baumert T.F., Ito S., Wong D.T., and Liang T.J. Hepatitis C virus structural proteins assemble into viruslike particles in insect cells. J. Virol. 72 (1998) 3827-3836
17. Branch A.D., Stump D.D., Gutierrez J.A., Eng F., and Walewski J.L. The hepatitis C virus alternate reading frame (ARF) and its family of novel products: the alternate reading frame protein/F-protein, the double-frameshift protein, and others. Semin. Liver Dis. 25 1 (2005) 105-117
18. Klein K.C., Polyak S.J., and Lingappa J.R. Unique features of hepatitis C virus capsid formation revealed by de novo cell-free assembly. J. Virol. 78 (2004) 9257-9269
19. Vauloup-Fellous C., Pene V., Garaud-Aunis J., Harper F., Bardin S., Suire Y., Pichard E., Schmitt A., Sogni P., Pierron G., Briand P., and Rosenberg A.R. Signal peptide peptidase-catalyzed cleavage of hepatitis C virus core protein is dispensable for virus budding but destabilizes the viral capsid. J. Biol. Chem. 281 (2006) 27679-27692
20. Pizzato M., Marlow S.A., Blair E.D., and Takeuchi Y. Initial binding of murine leukemia virus particles to cells does not require specific Env-receptor interaction. J. Virol. 73 (1999) 8599-8611
21. MacParland S.A., Pham T.N., Gujar S.A., and Michalak T.I. De novo infection and propagation of wild-type Hepatitis C virus in human T lymphocytes in vitro. J. Gen. Virol. 87 (2006) 3577-3586
22. Pham T.N., and Michalak T.I. Occult persistence and lymphotropism of hepatitis C virus infection. World J. Gastroenterol. 14 (2008) 2789-2793
23. Pham T.N., King D., Macparland S.A., McGrath J.S., Reddy S.B., Bursey F.R., and Michalak T.I. Hepatitis C virus replicates in the same immune cell subsets in chronic hepatitis C and occult infection. Gastroenterology 134 (2008) 812-822
24. Desai P., and Person S. Incorporation of the green fluorescent protein into the herpes simplex virus type 1 capsid. J. Virol. 72 (1998) 7563-7568
25. McDonald D., Vodicka M.A., Lucero G., Svitkina T.M., Borisy G.G., Emerman M., and Hope T.J. Visualization of the intracellular behavior of HIV in living cells. J. Cell Biol. 159 (2002) 441-452
26. Huang A.S., and Baltimore D. Defective viral particles and viral disease processes. Nature 226 (1970) 325-327
27. Lancaster M.U., Hodgetts S.I., Mackenzie J.S., and Urosevic N. Characterization of defective viral RNA produced during persistent infection of Vero cells with Murray Valley encephalitis virus. J. Virol. 72 (1998) 2474-2482
28. Yoon S.W., Lee S.Y., Won S.Y., Park S.H., Park S.Y., and Jeong Y.S. Characterization of homologous defective interfering RNA during persistent infection of Vero cells with Japanese encephalitis virus. Mol. Cells 21 (2006) 112-120
29. Kaito M., Watanabe M.S., Tsukiyama-Kohara K., Yamaguchi K., Kobayashi Y., Konishi M., Yokoi M., Ishida S., Suzuki S., and Kohara M. Hepatitis C virus particle detected by immunoelectron microscopic study. J. Gen. Virol. 75 (1994) 1755-1760
30. Kanto T., Hayashi T.N., Takehara T., Hagiwara H., Mita E., Naito M., Kasahara A., Fusamoto H., and Kamada T. Buoyant density of hepatitis C virus recovered from infected hosts: two different features in sucrose equilibrium density-gradient centrifugation related to degree of liver inflammation. Hepatology 19 (1994) 296-302
31. Pelkmans L., Kartenbeck J., and Helenius A. Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nat. Cell Biol. 3 (2001) 473-484
32. Ratinier M., Boulant S., Combet C., Targett-Adams P., McLauchlan J., and Lavergne J.P. Transcriptional slippage prompts recoding in alternate reading frames in the hepatitis C virus (HCV) core sequence from strain HCV-1. J. Gen. Virol. 89 (2008) 1569-1578
33. Shavinskaya A., Boulant S., Penin F., McLauchlan J., and Bartenschlager R. The lipid droplet binding domain of hepatitis C virus core protein is a major determinant for efficient virus assembly. J. Biol. Chem. 282 51 (2007) 37158-37169
34. Dundr M., McNally J., Cohen J., and Misteli T. Quantitation of GFP-fusion proteins in single living cells. J. Struct. Biol. 140 (2002) 92-99
35. Aaskov J., Buzacott K., Thu H.M., Lowry K., and Holmes E.C. Long-term transmission of defective RNA viruses in humans and Aedes mosquitoes. Science 311 (2006) 236-238
36. L. Pacini, R. Graziani, L. Bartholomeu, R. De Francesco, G. Paonessa, Hepatitis C virus sub-genomic RNA resembling natural occurring deletion mutants are efficiently trans-packaged into virus-like particles by helper virus or helper cell lines. In: Abstract presented in 15th International Symposium on Hepatitis C virus & Related Viruses, (2008) San Antonio Texas.
37. Duvignaud J.B., Davard C., Fromentin R., Majeau N., Leclerc D., and Gagne S. Structure and dynamics of the N-terminal half of hepatitis C virus core protein: an intrinsically unstructured protein. Biochem. Res. Commun. 378 1 (2009) 27-31
38. F. Eng, A.L. Klepper, J. Walewski, S.L. Fishman, L. McMullan, M.J. Evans, C.M. Rice, S. Desai, A.D. Branch, The hepatitis C virus core gene expresses a family of N-terminally truncated isoforms of the nucleocapsid (core) protein. In: Abstract presented in 15th International Symposium on Hepatitis C virus & Related Viruses, (2008) San Antonio Texas.
39. Mark J., Li X., Cyr T., Fournier S., Jaentschke B., and Hefford M.A. SARS coronavirus: unusual lability of the nucleocapsid protein. Biochem. Res. Commun. 377 2 (2008) 429-433
40. Falcón V., Acosta-Rivero N., Chinea G., and 12 other authors. Ultrastructural evidences of HCV infection in hepatocytes of chronically HCV-infected patients. Biochem. Biophys. Res. Commun. 305 (2003) 1085-1090
41. Kondo Y., Sung V.M.H., Machida K., Liu M., and Lai M.M.C. Hepatitis C infects T cells and affects interferon -γ signaling in T cell lines. Virology 361 (2007) 161-173
42. Helenius A., Kartenbeck J., Simons K., and Fries E. On the entry of Semliki forest virus into BHK-21 cells. J. Cell Biol. 84 (1980) 404-420
43. Eng F., Klepper A.L., Walewski J., Fishman S.L., Desai S., McMullan L., Evans M.J., Rice C.M., and Branch A.D. Internal initiation stimulates production of p8 mini-core, a member of a newly discovered family of hepatitis C virus core protein isoforms. J. Virol. 83 (2009) 3104-3114
44. Le Gallic L., Virgilio L., Cohen P., Biteau B., and Mavrothalassitis G. ERF nuclear shuttling, a continuous monitor of ERK activity that links it to cell cycle progression. Mol. Cell Biol. 24 (2004) 1206-1218